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Food-borne illnesses can be classified as infections, where the consumer ingests foods containing live organisms mostly in large numbers, or intoxications, where the consumer ingests food containing preformed toxins. However, only food-borne pathogens of major importance are discussed briefly in this review due to their higher incidence and importance in meat products. Comprehensive reviews on these pathogens and their thermal destruction characteristics can be found in a treatise by the International Commission for Microbiological Specification of Foods (ICMSF).20 Similarly, recent incidents of foot-and-mouth disease and bovine spongi- form encephalopathy in cattle indictate that new safety issues will arise in the future. The focus of this section will be on bacterial pathogens of significance in meat products and their destruction during thermal processing in combination with other methodologies. The pathogens of concern in meat products include E.

coli O157:H7, Salmonella spp., L. monocytogenes, S. aureus, and Clostridium

6.5.2.1 Escherichia coli O157:H7

E. coli O157:H7 is considered a pathogen of significance in beef and ground beef

products. Recently, E. coli O157:H7 and other enterohemorrhagic E. coli have emerged as prominent food-borne disease agents. Cattle are a reservoir of E. coli O157:H7, and the consumption of raw or undercooked beef has most often been associated with food-borne infections. Therefore, during the processing of meat products, thermal processes should be designed to eliminate this pathogen. Because this pathogen has similar growth and lethality characteristics as Salmo-

nella spp., thermal processes developed for meat products target the elimination

of Salmonella spp. rather than E. coli O157:H7. Similarly, pathogen modeling programs consider using Salmonella spp. as an indicator organism to model the survival/growth of this pathogen. USDA-FSIS based the lethality performance standards for processed products on this assumption.27,28 D and Z values for E. coli O157:H7 had been determined in ground beef.29

6.5.2.2 Salmonella spp.

Salmonella spp. is widely distributed in nature and is a major cause of food-borne

illness in the U.S., and >95% of the nontyphoidal Salmonella outbreaks are food- borne.30 The growth rate of Salmonella spp. is substantially reduced at <15°C, while growth of most Salmonella spp. is prevented below 7°C. Maximal growth rates for Salmonella spp. are reported at 49.5°C.19 The U.S. Department of Agriculture published lethality performance standards for certain processed meat and poultry products that prescribe Salmonella spp. reductions to be attained during processing.27,28 These lethality standards require a 6.5 log destruction of

Salmonella spp. during processing of prepared meat products, and a 7.0 log

destruction of Salmonella spp. is required for products containing poultry meat.

6.5.2.3 Listeria monocytogenes

Listeria spp. is ubiquitous in nature. The organism is commonly found in the

intestines of animals and humans without causing illness. It can survive for long periods of time in soil, leaf litter, sewage, silage dust, vegetation, and water. The organism has been isolated from a variety of products, including raw milk, cheese made from unpasteurized milk, soft cheese, meat and poultry and their products, cole slaw, and cabbage. L. monocytogenes grows under low-oxygen conditions at refrigeration temperatures and survives for long periods in the environment, on foods, in processing plants, and in household refrigerators. Although frequently present in raw foods of both plant and animal origin, it can also be present in cooked foods because of postprocessing contamination. Consumption of food contaminated with L. monocytogenes can cause listeriosis.

According to the U.S. Centers for Disease Control and Prevention (CDC),

L. monocytogenes causes an estimated 2493 cases of listeriosis per year. Of

these, 2298 persons are hospitalized and 499 persons die.30 The case fatality rate is high across the whole population — 20 deaths per 100 cases of illness.

Epidemiologic surveillance data indicate that the case fatality rate varies by age, with a higher case fatality rate among newborns and the elderly.

L. monocytogenes can be in the food processing environment and can form

biofilms on solid surfaces commonly found in food processing plants, including stainless steel and rubber under experimental conditions. Listeria can also survive adverse conditions on apparently smooth surfaces. Recently, several recalls of ready- to-eat (RTE) meat and poultry products have occurred because of adulteration with

L. monocytogenes. Food-borne illnesses and deaths have been linked to some recalled

products. It has generally been concluded that the adulteration occurred through cross-contamination from environmental sources following cooking.

6.5.2.4 Clostridium perfringens

C. perfringens is widely distributed in a variety of foods, particularly meat and

poultry, and has been implicated in numerous food-borne disease outbreaks. The abilities of C. perfringens to form heat-resistant spores and grow at a very rapid rate at relatively high temperatures are the major contributing factors leading to food poisoning. The temperature range for growth of C. perfringens, 6 to 52.3°C is well documented.20,31 A short generation time of 7.1 min in ground beef means that after the spores have germinated, rapid cooling of foods is critical.1,32,33

C. perfringens continues to be a concern to the food industry, particularly to

the retail and food service industries, and has been implicated in several large outbreaks. The U.S. Centers for Disease Control and Prevention estimates more than 248,000 cases of food-borne illness due to C. perfringens annually in the U.S.30 Although C. perfringens vegetative cells do not survive the normal heat processing schedules employed in the meat industry, the spores can survive. Heat- activated spores can germinate and grow rapidly if these products are improperly chilled. Juneja and coworkers1,32,33 reported D

58°C values of 1.15 to 1.60 min for 10 strains of C. perfringens (vegetative cells) in a model beef gravy system, which are similar to the D values reported for vegetative food-borne pathogens such as

E. coli O157:H7, Salmonella spp., and L. monocytogenes.29,34 Lethality standards for Salmonella spp.27,28 should be adequate to control normal incidence levels of

C. perfringens vegetative cells in processed meat and poultry products.

In case thermal process deviations (heating or cooling) occur, spores of C.

perfringens, if present in the raw meats utilized for processing of cooked products

may be heat activated, germinate, and grow to hazardous levels during cooling or improper storage. The time/temperature guidelines for cooling cooked products specify that the maximum internal temperature should not remain between 54.4 and 26.7°C for more than 1.5 h, nor between 26.7 and 4.4°C for more than 5 h.28 The U.S. Food and Drug Administration (FDA) Division of Retail Food Protection recognized that inadequate cooling was a major food safety problem and estab- lished a recommendation that all food should be cooled from 60 to 21°C in 2 h and from 21 to 5°C in 4 h.35 Of importance is the use of organic acid antimicrobials such as lactates, diacetates, and citrates, which have been shown to act as bacteriostats to prevent outgrowth of activated spores.36 A complete compilation

of studies determining the survival and growth of C. perfringens spores during thermal processing of meats is available.37

6.5.2.5 Staphylococcus aureus

S. aureus is ubiquitous and is common in the mucous membranes and skin of most

warm-blooded animals, including food animals. S. aureus is an opportunistic patho- gen, cannot compete well with other food spoilage bacteria, and can grow and cause illness in cooked foods that are cross-contaminated. Although staphylococci are readily destroyed by the temperatures normally used for processing of meat and poultry products, growth of the organisms to levels greater than 5.0 log CFU/g can result in production of extremely heat stable enterotoxins, which can survive even commercial sterilization processes. The organism is resistant to drying and may grow and produce enterotoxins in products having aw as low as 0.85. It is very resistant to freezing and thawing and survives well in frozen meat products.20

The CDC estimates approximately 185,000 cases of staphylococcal illness annually and 100% of the outbreaks are food-borne.30 Although S. aureus is not part of the lethality and stabilization performance standards for cooked ready-to- eat products, the ability of the organism to elaborate heat-stable toxins that can survive subsequent cooking contribute to its importance during thermal process- ing of meat products.

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